Targeting carcinoma-associated fibroblasts within the tumor stroma with a fibroblast activation protein-activated prodrug

Journal of the National Cancer Institute

Volumn 104, Issue 17, 2012, Pages 1320-1334

  Brennen, W Nathaniel ^a   Rosen, D Marc ^b   Wang, Hao ^b   Isaacs, John T ^b   Denmeade, Samuel R ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 O (12 AMINODODECANOYL) 8 O DEBUTANOYL THAPSIGARGIN; FIBROBLAST ACTIVATION PROTEIN; MEMBRANE PROTEIN; THAPSIGARGIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CALCIUM CELL LEVEL; CANCER CELL; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; IC 50; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN TARGETING; STROMA CELL; TUMOR GROWTH; TUMOR VOLUME;

AMINO ACIDS; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CALCIUM; CELL LINE, TUMOR; FEMALE; GELATINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; NEOPLASMS; PRODRUGS; PROSTATIC NEOPLASMS; SERINE ENDOPEPTIDASES; THAPSIGARGIN; TRANSPLANTATION, HETEROLOGOUS; TUMOR MARKERS, BIOLOGICAL; URINARY BLADDER NEOPLASMS;

EID: 84866096019     PISSN: 00278874     EISSN: 14602105     Source Type: Journal    
DOI: 10.1093/jnci/djs336     Document Type: Article

References (67)

1. Bast R Jr, Kufe DW, Pollock RE, Weichselbaum RR, Holland JF, Frei E III, Gansler TS. Cancer Medicine. 5th ed. Hamilton, ON: BC Decker; 2000.
2. Hewitt RE, Powe DG, Carter GI, Turner DR. Desmoplasia and its relevance to colorectal tumour invasion. Int J Cancer. 1993;53(1):62-69. (Pubitemid 23018424)
3. Rønnov-Jessen L, Petersen OW, Bissell MJ. Cellular changes involved in conversion of normal to malignant breast: importance of the stromal reaction. Physiol Rev. 1996;76(1):69-125. (Pubitemid 26048279)
4. Mueller MM, Fusenig NE. Friends or foes\-bipolar effects of the tumour stroma in cancer. Nat Rev Cancer. 2004;4(11):839-849. (Pubitemid 39472951)
5. Allinen M, Beroukhim R, Cai L, et al. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell. 2004;6(1):17-32. (Pubitemid 38903159)
6. Franco OE, Shaw AK, Strand DW, Hayward SW. Cancer associated fibro-blasts in cancer pathogenesis. Semin Cell Dev Biol. 2010;21(1):33-39.
7. Shimoda M, Mellody KT, Orimo A. Carcinoma-associated fibroblasts are a rate-limiting determinant for tumour progression. Semin Cell Dev Biol. 2010;21(1):19-25.
8. Ostman A, Augsten M. Cancer-associated fibroblasts and tumor growth- bystanders turning into key players. Curr Opin Genet Dev. 2009;19(1):67-73.
9. Loeffler M, Krüger JA, Niethammer AG, Reisfeld RA. Targeting tumor-associated fibroblasts improves cancer chemotherapy by increasing intratumoral drug uptake. J Clin Invest. 2006;116(7):1955-1962. (Pubitemid 44033319)
10. Kraman M, Bambrough PJ, Arnold JN, et al. Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-alpha. Science. 2010;330(6005):827-830.
11. Brennen WN, Isaacs JT, Denmeade SR. Rationale behind targeting fibro-blast activation protein-expressing carcinoma-associated fibroblasts as a novel chemotherapeutic strategy. Mol Cancer Ther. 2012;11(2):257-266.
12. Garin-Chesa P, Old LJ, Rettig WJ. Cell surface glycoprotein of reactive stromal fibroblasts as a potential antibody target in human epithelial cancers. Proc Natl Acad Sci USA. 1990;87(18):7235-7239.
13. O'Brien P, O'Connor BF. Seprase: an overview of an important matrix serine protease. Biochim Biophys Acta. 2008;1784(9):1130-1145.
14. Yu DM, Yao TW, Chowdhury S, et al. The dipeptidyl peptidase IV family in cancer and cell biology. FEBS J. 2010;277(5):1126-1144.
15. Edosada CY, Quan C, Tran T, et al. Peptide substrate profiling defines fibroblast activation protein as an endopeptidase of strict Gly(2)-Pro(1)- cleaving specificity. FEBS Lett. 2006;580(6):1581-1586. (Pubitemid 43290354)
16. Park JE, Lenter MC, Zimmermann RN, Garin-Chesa P, Old LJ, Rettig WJ. Fibroblast activation protein, a dual specificity serine protease expressed in reactive human tumor stromal fibroblasts. J Biol Chem. 1999;274(51):36505-36512.
17. Aggarwal S, Brennen WN, Kole T P, et al. Fibroblast activation protein peptide substrates identified from human collagen I derived gelatin cleavage sites. Biochemistry. 2008;47(3):1076-1086.
18. Christiansen VJ, Jackson KW, Lee KN, McKee PA. Effect of fibroblast activation protein and alpha2-antiplasmin cleaving enzyme on collagen types I, III, and I V. Arch Biochem Biophys. 2007;457(2):177-186. (Pubitemid 46048698)
19. Tuxhorn JA, Ayala GE, Smith MJ, Smith VC, Dang TD, Rowley DR. Reactive stroma in human prostate cancer: induction of myofibroblast phenotype and extracellular matrix remodeling. Clin Cancer Res. 2002;8(9):2912-2923. (Pubitemid 35025739)
20. Cohen SJ, Alpaugh RK, Palazzo I, et al. Fibroblast activation protein and its relationship to clinical outcome in pancreatic adenocarcinoma. Pancreas. 2008;37(2):154-158.
21. Henry LR, Lee HO, Lee JS, et al. Clinical implications of fibro-blast activation protein in patients with colon cancer. Clin Cancer Res. 2007;13(6):1736-1741. (Pubitemid 46952939)
22. Bae S, Park CW, Son HK, et al. Fibroblast activation protein alpha identifies mesenchymal stromal cells from human bone marrow. Br J Haematol. 2008;142(5):827-830.
23. Scanlan MJ, Raj BK, Calvo B, et al. Molecular cloning of fibroblast activation protein alpha, a member of the serine protease family selectively expressed in stromal fibroblasts of epithelial cancers. Proc Natl Acad Sci USA. 1994;91(12):5657-5661. (Pubitemid 24174387)
24. Acharya PS, Zukas A, Chandan V, Katzenstein AL, Puré E. Fibroblast activation protein: a serine protease expressed at the remodeling interface in idiopathic pulmonary fibrosis. Hum Pathol. 2006;37(3):352-360. (Pubitemid 43277524)
25. Levy MT, McCaughan GW, Abbott CA, et al. Fibroblast activation protein: a cell surface dipeptidyl peptidase and gelatinase expressed by stellate cells at the tissue remodelling interface in human cirrhosis. Hepatology. 1999;29(6):1768-1778. (Pubitemid 29247051)
26. Rettig WJ, Garin-Chesa P, Healey JH, et al. Regulation and hetero-meric structure of the fibroblast activation protein in normal and transformed cells of mesenchymal and neuroectodermal origin. Cancer Res. 1993;53(14):3327-3335. (Pubitemid 23223305)
27. Campbell I, Polyak K, Haviv I. Clonal mutations in the cancer-associated fibroblasts: the case against genetic coevolution. Cancer Res. 2009;69(17):6765- 6768; discussion 6769.
28. Puré E. The road to integrative cancer therapies: emergence of a tumor-associated fibroblast protease as a potential therapeutic target in cancer. Expert Opin Ther Targets. 2009;13(8):967-973.
29. Edosada CY, Quan C, Wiesmann C, et al. Selective inhibition of fibroblast activation protein protease based on dipeptide substrate specificity. J Biol Chem. 2006;281(11):7437-7444. (Pubitemid 43847515)
30. Gibson F, Singh AK, Soumeillant MC, Manchand PS, Humora M, Kronenthal DR. A practical synthesis of l-valyl-pyrrolidine-(2R)-boronic acid: efficient recycling of the costly chiral auxiliary (+)-pinanediol. Org. Process Res Dev. 2002;6(6):814-816.
31. Denmeade SR, Jakobsen CM, Janssen S, et al. Prostate-specific antigen-activated thapsigargin prodrug as targeted therapy for prostate cancer. J Natl Cancer Inst. 2003;95(13):990-1000. (Pubitemid 36896716)
32. Tombal B, Denmeade SR, Isaacs JT. Assessment and validation of a microinjection method for kinetic analysis of [Ca2+]i in individual cells undergoing apoptosis. Cell Calcium. 1999;25(1):19-28. (Pubitemid 29083988)
33. Denmeade SR, Lin XS, Tombal B, Isaacs JT. Inhibition of caspase activity does not prevent the signaling phase of apoptosis in prostate cancer cells. Prostate. 1999;39(4):269-279. (Pubitemid 29244501)
34. Mancuso MR, Davis R, Norberg SM, et al. Rapid vascular regrowth in tumors after reversal of VEGF inhibition. J Clin Invest. 2006;116(10): 2610-2621. (Pubitemid 44511625)
35. Hammers HJ, Verheul HM, Salumbides B, et al. Reversible epithelial to mesenchymal transition and acquired resistance to sunitinib in patients with renal cell carcinoma: evidence from a xenograft study. Mol Cancer Ther. 2010;9(6):1525-1535.
36. Janssen S, Rosen DM, Ricklis RM, et al. Pharmacokinetics, biodistribution, and antitumor efficacy of a human glandular kallikrein 2 (hK2)-activated thapsigargin prodrug. Prostate. 2006;66(4):358-368. (Pubitemid 43346946)
37. Sivridis E, Giatromanolaki A, Koukourakis MI. Proliferating fibroblasts at the invading tumour edge of colorectal adenocarcinomas are associated with endogenous markers of hypoxia, acidity, and oxidative stress. J Clin Pathol. 2005;58(10):1033-1038. (Pubitemid 41416051)
38. Hasebe T, Sasaki S, Sugitoh M, Ono M, Saitoh N, Ochiai A. Proliferative activities of tumor stromal cells play important roles in tumor thickness and progression of T3 ulcerative-type colorectal cancer. Virchows Arch. 2003;442(6):569-576. (Pubitemid 36819251)
39. Fox SB, Gatter KC, Bicknell R, et al. Relationship of endothelial cell proliferation to tumor vascularity in human breast cancer. Cancer Res. 1993;53(18):4161-4163. (Pubitemid 24146759)
40. Lytton J, Westlin M, Hanley MR. Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J Biol Chem. 1991;266(26):17067-17071. (Pubitemid 21907906)
41. Furuya Y, Lundmo P, Short AD, Gill DL, Isaacs JT. The role of calcium, pH, and cell proliferation in the programmed (apoptotic) death of androgen-independent prostatic cancer cells induced by thapsigargin. Cancer Res. 1994;54(23):6167-6175.
42. Denmeade SR, Isaacs JT. The SERCA pump as a therapeutic target: making a "smart bomb" for prostate cancer. Cancer Biol Ther. 2005;4(1):14-22. (Pubitemid 41350924)
43. Lin XS, Denmeade SR, Cisek L, Isaacs JT. Mechanism and role of growth arrest in programmed (apoptotic) death of prostatic cancer cells induced by thapsigargin. Prostate. 1997;33(3):201-207. (Pubitemid 27509421)
44. Thastrup O, Cullen PJ, Drøbak BK, Hanley MR, Dawson A P. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci USA. 1990;87(7):2466-2470.
45. Sagara Y, Inesi G. Inhibition of the sarcoplasmic reticulum Ca2+ transport ATPase by thapsigargin at subnanomolar concentrations. J Biol Chem. 1991;266(21):13503-13506. (Pubitemid 21907377)
46. Davidson GA, Varhol RJ. Kinetics of thapsigargin-Ca(2+)-ATPase (sarco-plasmic reticulum) interaction reveals a two-step binding mechanism and picomolar inhibition. J Biol Chem. 1995;270(20):11731-11734.
47. Jakobsen CM, Denmeade SR, Isaacs JT, Gady A, Olsen CE, Christensen SB. Design, synthesis, and pharmacological evaluation of thapsigargin analogues for targeting apoptosis to prostatic cancer cells. J Med Chem. 2001;44(26):4696- 4703. (Pubitemid 33144479)
48. Collins PJ, McMahon G, O'Brien P, O'Connor B. Purification, identification and characterisation of seprase from bovine serum. Int J Biochem Cell Biol. 2004;36(11):2320-2333. (Pubitemid 39094452)
49. Lee KN, Jackson KW, Christiansen VJ, Chung KH, McKee PA. A novel plasma proteinase potentiates alpha2-antiplasmin inhibition of fibrin digestion. Blood. 2004;103(10):3783-3788. (Pubitemid 38596296)
50. Lee KN, Jackson KW, Christiansen VJ, Lee CS, Chun JG, McKee PA. Antiplasmin-cleaving enzyme is a soluble form of fibroblast activation protein. Blood. 2006;107(4):1397-1404. (Pubitemid 43242374)
51. Santos AM, Jung J, Aziz N, Kissil JL, Puré E. Targeting fibroblast activation protein inhibits tumor stromagenesis and growth in mice. J Clin Invest. 2009;119(12):3613-3625.
52. Ostermann E, Garin-Chesa P, Heider KH, et al. Effective immunoconju-gate therapy in cancer models targeting a serine protease of tumor fibro-blasts. Clin Cancer Res. 2008;14(14):4584-4592.
53. Scott AM, Wiseman G, Welt S, et al. A phase I dose-escalation study of sibrotuzumab in patients with advanced or metastatic fibroblast activation protein-positive cancer. Clin Cancer Res. 2003;9(5):1639-1647. (Pubitemid 36554586)
54. Eager RM, Cunningham CC, Senzer N, et al. Phase II trial of talabostat and docetaxel in advanced non-small cell lung cancer. Clin Oncol (R Coll Radiol). 2009;21(6):464-472.
55. Hofheinz RD, al-Batran SE, Hartmann F, et al. Stromal antigen targeting by a humanised monoclonal antibody: an early phase II trial of sibrotuzumab in patients with metastatic colorectal cancer. Onkologie. 2003;26(1):44-48. (Pubitemid 36302438)
56. Messerschmidt SK, Musyanovych A, Altvater M, et al. Targeted lipid-coated nanoparticles: delivery of tumor necrosis factor-functionalized particles to tumor cells. J Control Release. 2009;137(1):69-77.
57. Samel D, Muller D, Gerspach J, et al. Generation of a FasL-based proa-poptotic fusion protein devoid of systemic toxicity due to cell-surface antigen-restricted Activation. J Biol Chem. 2003;278(34):32077-32082. (Pubitemid 37048396)
58. Wang XM, Yao TW, Nadvi NA, Osborne B, McCaughan GW, Gorrell MD. Fibroblast activation protein and chronic liver disease. Front Biosci. 2008;13:3168-3180. (Pubitemid 351589228)
59. Bauer S, Jendro MC, Wadle A, et al. Fibroblast activation protein is expressed by rheumatoid myofibroblast-like synoviocytes. Arthritis Res Ther. 2006;8(6):R171.
60. Dohi O, Ohtani H, Hatori M, et al. Histogenesis-specific expression of fibroblast activation protein and dipeptidylpeptidase-IV in human bone and soft tissue tumours. Histopathology. 2009;55(4):432-440.
61. Juillerat-Jeanneret L, Gerber-Lemaire S. The prolyl-aminodipeptidases and their inhibitors as therapeutic targets for fibrogenic disorders. Mini Rev Med Chem. 2009;9(2):215-226.
62. Cheng JD, Dunbrack RL Jr, Valianou M, Rogatko A, Alpaugh RK, Weiner LM. Promotion of tumor growth by murine fibroblast activation protein, a serine protease, in an animal model. Cancer Res. 2002;62(16):4767-4772.
63. Liao D, Luo Y, Markowitz D, Xiang R, Reisfeld RA. Cancer associated fibroblasts promote tumor growth and metastasis by modulating the tumor immune microenvironment in a 4T1 murine breast cancer model. PLoS ONE. 2009;4(11):e7965.
64. Huang Y, Wang S, Kelly T. Seprase promotes rapid tumor growth and increased microvessel density in a mouse model of human breast cancer. Cancer Res. 2004;64(8):2712-2716. (Pubitemid 38500606)
65. Ramirez-Montagut T, Blachere NE, Sviderskaya EV, et al. FAPalpha, a surface peptidase expressed during wound healing, is a tumor suppressor. Oncogene. 2004;23(32):5435-5446. (Pubitemid 39044054)
66. Ariga N, Sato E, Ohuchi N, Nagura H, Ohtani H. Stromal expression of fibroblast activation protein/seprase, a cell membrane serine proteinase and gelatinase, is associated with longer survival in patients with invasive ductal carcinoma of breast. Int J Cancer. 2001;95(1):67-72.
67. Vander Griend DJ, Antony L, Dalrymple SL, et al. Amino acid containing thapsigargin analogues deplete androgen receptor protein via synthesis inhibition and induce the death of prostate cancer cells. Mol Cancer Ther. 2009;8(5):1340-1349.